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日常拥挤应激对手术标记大西洋鲑(Salmo salar)皮肤和头肾基因表达有有限但可检测的影响。

Daily crowding stress has limited, yet detectable effects on skin and head kidney gene expression in surgically tagged atlantic salmon (Salmo salar).

机构信息

Faculty of Biosciences and Aquaculture, Nord University, BODØ, Norway.

Faculty of Biosciences and Aquaculture, Nord University, BODØ, Norway.

出版信息

Fish Shellfish Immunol. 2024 Sep;152:109794. doi: 10.1016/j.fsi.2024.109794. Epub 2024 Jul 30.

DOI:10.1016/j.fsi.2024.109794
PMID:39089638
Abstract

To ensure welfare-friendly and effective internal tagging, the tagging process should not cause a long-term burden on individuals given that tagged fish serve as representatives for the entire population in telemetry applications. To some extent, stress is inevitable within regular aquaculture practices, and thus, the consequences of long-term stress should be described in terms of their effects on internal tagging. In fish, stressors activate the Hypothalamus-Pituitary-Interrenal (HPI) and Brain-Sympathetic-Chromaffin Cell (BSC) axes, leading to neuroimmunoendocrine communication and paracrine interactions among stress hormones. The interrelation between wound healing and stress is complex, owing to their shared components, pathways, and energy demands. This study assessed 14 genes (mmp9, mmp13, il-2, il-4, il-8a, il-10, il-12, il-17d, il-1b, tnfa, ifng, leg-3, igm, and crh) in the skin (1.5 cm from the wound) and head kidney over eight weeks. These genes, associated with cell signaling in immunity, wound healing, and stress, have previously been identified as influenced and regulated by these processes. Half of a group of Atlantic salmon (n = 90) with surgically implanted dummy smart-tags were exposed to daily crowding stress. The goal was to investigate how this gene panel responds to a wound alone and then to the combined effects of wounding and daily crowding stress. Our observations indicate that chronic stress impacts inflammation and impedes wound healing, as seen through the expression of matrix metalloproteinases genes in the skin but not in the head kidney. This difference is likely due to the ongoing internal wound repair, in contrast to the externally healed wound incision. Cytokine expression, when significant in the skin, was mainly downregulated in both treatments compared to control values, particularly in the study's first half. Conversely, the head kidney showed initial cytokine downregulation followed by upregulation. Across all weeks observed and combining both tissues, the significantly expressed gene differences were 12 % between the Wound and Stress groups, 28 % between Wound and Control, and 25 % between Stress and Control. Despite significant fluctuations in cytokines, sustained variations across multiple weeks are only evident in a few select genes. Furthermore, Stress individuals demonstrated the most cytokine correlations within the head kidney, which may suggest that chronic stress affects cytokine expression. This investigation unveils that the presence of stress and prolonged activation of the HPI axis in an eight weeklong study has limited yet detectable effects on the selected gene expression within immunity, wound healing, and stress, with notable tissue-specific differences.

摘要

为了确保对福利友好且有效的内部标记,标记过程不应给个体带来长期负担,因为标记的鱼类在遥测应用中代表整个种群。在某种程度上,压力在常规水产养殖实践中是不可避免的,因此,应根据其对内标记的影响来描述长期压力的后果。在鱼类中,应激源激活下丘脑-垂体-肾上腺(HPI)和脑交感-肾上腺髓质(BSC)轴,导致神经免疫内分泌通讯和应激激素的旁分泌相互作用。伤口愈合和应激之间的相互关系很复杂,因为它们有共同的组成部分、途径和能量需求。本研究在 8 周内评估了皮肤(距伤口 1.5 厘米处)和头肾中的 14 种基因(mmp9、mmp13、il-2、il-4、il-8a、il-10、il-12、il-17d、il-1b、tnfa、ifng、leg-3、igm 和 crh)。这些与免疫、伤口愈合和应激中的细胞信号相关的基因之前已被确定为受这些过程影响和调节。一组接受过手术植入假智能标记的大西洋鲑鱼(n=90)中有一半被暴露于日常拥挤应激下。目的是研究单独的伤口以及伤口和日常拥挤应激的联合效应对该基因谱的影响。我们的观察表明,慢性应激会影响炎症并阻碍伤口愈合,这可以通过皮肤中基质金属蛋白酶基因的表达来观察,但在头肾中则无法观察到。这种差异可能是由于正在进行的内部伤口修复,而不是外部愈合的伤口切口。细胞因子的表达在皮肤中有显著变化时,与对照值相比,在两种处理中均主要下调,尤其是在研究的前半部分。相反,头肾显示出初始细胞因子下调,随后上调。在所有观察到的周数和合并两种组织中,Wound 和 Stress 组之间的显著表达基因差异为 12%,Wound 和 Control 组之间为 28%,Stress 和 Control 组之间为 25%。尽管细胞因子有显著波动,但在数周内持续变化仅在少数选定基因中可见。此外,Stress 个体在头肾中显示出最多的细胞因子相关性,这可能表明慢性应激会影响细胞因子表达。这项研究揭示了在 8 周的研究中,压力的存在和 HPI 轴的长期激活对内选择基因表达在免疫、伤口愈合和应激方面的影响有限但可检测,且具有明显的组织特异性差异。

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